Abstract
Main conclusion
Camelina biotypes had different responses to freezing stress, which was mainly inherited by additive gene effects and can be reliably used in breeding programs and for a better understanding of freezing tolerance mechanisms in camelina plants.
Abstract
Camelina [Camelina sativa (L.) Crantz] is a frost-tolerant oilseed plant that is cultivated as an autumn crop in semi-arid regions. However, camelina establishment in these areas is limited by low temperatures in winter that results in decreased seed yield. In the present study, genetic basis of freezing tolerance (FT) in spring and winter biotypes of camelina was analyzed at seedling stage using a diallel cross experiment. The parents consisted of two winter doubled haploid (DH) lines with high (DH34 and DH31), two spring lines with medium (DH19 and DH26), and two spring lines with low FT (DH08 and DH91). For this purpose, the parents along with F1 entries were subjected to freezing stress and survival percentage, electrolyte leakage, and lethal temperature for 50% mortality (LT50) of the lines were measured. Results showed that although both additive and non-additive effects of the genes determine the FT, further analyses indicated that it was mainly controlled by the additive effects. Therefore, selection-based methods may be more efficient for improving FT in camelina genotypes. The results of specific combining ability (SCA) and heterosis analysis among various DH lines suggested that more tolerant cultivars of camelina could be developed by targeted crossings. When a tolerant winter line and a susceptible spring line were crossed, their progenies showed a higher FT compared with the progenies of a cross between two susceptible spring lines indicating FT is controlled by additive effects of the genes in camelina plants. These findings provided new insight into the genetic basis of freezing-related traits in camelina and could be used for more sophisticated breeding programs.
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Data availability
The datasets analyzed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- FT:
-
Freezing tolerance
- DH:
-
Doubled haploid
- GCA:
-
General combining ability
- LT50 :
-
Lethal temperature for 50% mortality
- SCA:
-
Specific combining ability
References
Aiswarya CS, Vijeth S, Sreelathakumary I, Kaushik P (2020) Diallel analysis of chilli pepper (Capsicum annuum L.) genotypes for morphological and fruit biochemical traits. Plants 9(1):1–15. https://doi.org/10.3390/plants9010001
Allen BL, Vigil MF, Jabro JD (2014) Camelina growing degree hour and base temperature requirements. Agron J 106(3):940–944. https://doi.org/10.2134/agronj13.0469
Anderson JV, Horvath DP, Doğramaci M, Dorn KM, Chao WS, Watkin EE, Hernandez AG, Marks MD, Gesch R (2018) Expression of FLOWERING LOCUS C and a frameshift mutation of this gene on chromosome 20 differentiate a summer and winter annual biotype of Camelina sativa. Plant Direct 2(7):e00060. https://doi.org/10.1002/pld3.60
Augustyniak A, Pawłowicz I, Lechowicz K, Izbiańska-Jankowska K, Arasimowicz-Jelonek M, Rapacz M, Perlikowski D, Kosmala A (2020) Freezing tolerance of Lolium multiflorum/Festuca arundinacea introgression forms is associated with the high activity of antioxidant system and adjustment of photosynthetic activity under cold acclimation. Int J Mol Sci 21(16):5899. https://doi.org/10.3390/ijms21165899
Beyene Y, Mugo S, Semagn K, Asea G, Trevisan W, Tarekegne A, Tefera T, Gethi J, Kiula B, Gakunga J, Karaya H (2013) Genetic distance among doubled haploid maize lines and their testcross performance under drought stress and non-stress conditions. Euphytica 192(3):379–392. https://doi.org/10.1007/s10681-013-0867-5
Borghi M, Xie D (2018) Cloning and characterization of a monoterpene synthase gene from flowers of Camelina sativa. Planta 247:443–457. https://doi.org/10.1007/s00425-017-2801-x
Bouchetat F, Aissat A (2019) Evaluation of the genetic determinism of an F1 generation of barley resulting from a complete diallel cross between autochthones and introduced cultivars. Heliyon 5(11):e02744. https://doi.org/10.1016/j.heliyon.2019.e02744
Coelho IF, Alves RS, Peixoto MA, Teodoro LPR, Teodoro PE, Pinto JFN, dos Reis EF, Bhering LL (2020) Multi-trait multi-environment diallel analyses for maize breeding. Euphytica 216(9):1–17. https://doi.org/10.1007/s10681-020-02677-9
do Rego ER, do Rego MM (2016) Genetics and breeding of chili pepper Capsicum spp. Production and breeding of chilli peppers (Capsicum spp.). Springer, Cham, pp 57–80. https://doi.org/10.1007/978-3-319-06532-8_4
Dragov R (2020) Determination of genetic parameters for inheritance of grain protein content in durum wheat. Cereal Res Commun 48:365–373. https://doi.org/10.1007/s42976-020-00044-x
Eunus AM, Johnson LPV, Aksel R (1962) Inheritance of winterhardiness in an eighteen-parent diallel cross of barley. Can J Genet Cytol 4:356–376. https://doi.org/10.1139/g62-046
Fiebelkorn D, Rahman M (2016) Development of a protocol for frost-tolerance evaluation in rapeseed/canola (Brassica napus L.). Crop J 4(2):147–152. https://doi.org/10.1016/j.cj.2015.11.004
Fiebelkorn D, Horvath D, Rahman M (2018) Genome-wide association study for electrolyte leakage in rapeseed/canola (Brassica napus L.). Mol Breed 38(11):129. https://doi.org/10.1007/s11032-018-0892-0
Fiust A, Rapacz M (2020) Downregulation of three novel candidate genes is important for freezing tolerance of field and laboratory cold acclimated barley. J Plant Physiol 244:153049. https://doi.org/10.1016/j.jplph.2019.153049
Georgieva K, Mihailova G, Veliechkova M, Popova A (2020) Recovery of photosynthetic activity of resurrection plant Haberlea rhodopensis from drought- and freezing-induced desiccation. Photosynthetica 58(4):911–921. https://doi.org/10.32615/ps.2020.044
Gesch RW, Archer DW (2013) Double-cropping with winter camelina in the northern Corn Belt to produce fuel and food. Ind Crops Prod 44:718–725. https://doi.org/10.1016/j.indcrop.2012.05.023
Hawkins GP, Deng Z, Kubik TJ, Johnson-Flanagan AM (2002) Characterization of freezing tolerance and vernalization in Vern-, a spring-type Brassica napus line derived from a winter cross. Planta 216:220–226. https://doi.org/10.1007/s00425-002-0850-1
Hoermiller II, Ruschhaupt M, Heyer AG (2018) Mechanisms of frost resistance in Arabidopsis thaliana. Planta 248:827–835. https://doi.org/10.1007/s00425-018-2939-1
Horvath D, Anderson JV, Chao WS, Zheng P, Buchwaldt M, Parkin IA, Dorn K (2019) Genes associated with chloroplasts and hormone-signaling, and transcription factors other than CBFs are associated with differential survival after low temperature treatments of Camelina sativa biotypes. PLoS ONE 14(5):e0217692. https://doi.org/10.1371/journal.pone.0217692
Kagale S, Koh C, Nixon J, Bollina V, Clarke WE, Tuteja R, Spillane C, Robinson SJ, Links MG, Clarke C, Higgins EE (2014) The emerging biofuel crop Camelina sativa retains a highly undifferentiated hexaploid genome structure. Nat Commun 5(1):1–11. https://doi.org/10.1038/ncomms4706
Kaushik P, Dhaliwal MS (2018) Diallel analysis for morphological and biochemical traits in tomato cultivated under the influence of tomato leaf curl virus. Agronomy 8(8):153. https://doi.org/10.3390/agronomy8080153
Kenga R, Alabi SO, Gupta SC (2004) Combining ability studies in tropical sorghum (Sorghum bicolor (L.) Moench). Field Crops Res 88(2–3):251–260. https://doi.org/10.1016/j.fcr.2004.01.002
Kim DH, Doyle MR, Sung S, Amasino RM (2009) Vernalization: winter and the timing of flowering in plants. Annu Rev Cell Dev Biol 25:277–299. https://doi.org/10.1146/annurev.cellbio.042308.113411
Kimball JA, Isleib TG, Reynolds WC, Zuleta MC, Milla-Lewis SR (2016) Combining ability for winter survival and turf quality traits in St. Augustinegrass. HortScience 51(7):810–815. https://doi.org/10.21273/HORTSCI.51.7.810
Kurasiak-Popowska D, Tomkowiak A, Człopińska M, Bocianowski J, Weigt D, Nawracała J (2018) Analysis of yield and genetic similarity of Polish and Ukrainian Camelina sativa genotypes. Ind Crops Prod 123:667–675. https://doi.org/10.1016/j.indcrop.2018.07.001
Kwak KJ, Kim HS, Jang HY, Kang H, Ahn SJ (2016) Diverse roles of glycine-rich RNA-binding protein 7 in the response of camelina (Camelina sativa) to abiotic stress. Acta Physiol Plant 38:129. https://doi.org/10.1007/s11738-016-2144-4
Larsen A (1994) Breeding winter hardy grasses. Euphytica 77:231–237. https://doi.org/10.1007/BF02262635
Makumbi D, Alvarado G, Crossa J, Burgueño J (2018) SASHAYDIALL: a SAS program for Hayman’s diallel analysis. Crop Sci 58(4):1605–1615. https://doi.org/10.2135/cropsci2018.01.0047
Mandakova T, Pouch M, Brock JR, Al-Shehbaz IA, Lysak MA (2019) Origin and evolution of diploid and allopolyploid Camelina genomes were accompanied by chromosome shattering. Plant Cell 31(11):2596–2612. https://doi.org/10.1105/tpc.19.00366
Mather K, Jinks JL (2013) Biometrical genetics: the study of continuous variation. Springer, New York
Matias FI, Barrios SCL, Bearari LM, Meireles KGX, Mateus RG, Amaral PNCD, Alves GF, Valle CBD, Fritsche-Neto R (2018) Contribution of additive and dominance effects on agronomical and nutritional traits, and multivariate selection on Urochloa spp. hybrids. Crop Sci 58(6):2444–2458. https://doi.org/10.2135/cropsci2018.04.0261
McClinchey SL, Kott LS (2008) Production of mutants with high cold tolerance in spring canola (Brassica napus). Euphytica 162:51–67. https://doi.org/10.1007/s10681-007-9554-8
Miah MAA, Earle ED, Khush GS (1985) Inheritance of callus formation ability in anther cultures of rice Oryza sativa L. Theor Appl Genet 70(2):113–116. https://doi.org/10.1007/bf00275308
Neupane D, Solomon JK, Mclennon E, Davison J, Lawry T (2020) Camelina production parameters response to different irrigation regimes. Ind Crops Prod 148:112286. https://doi.org/10.1016/j.indcrop.2020.112286
Righini D, Zanetti F, Martínez-Force E, Mandrioli M, Toschi TG, Monti A (2019) Shifting sowing of camelina from spring to autumn enhances the oil quality for bio-based applications in response to temperature and seed carbon stock. Ind Crops Prod 137:66–73. https://doi.org/10.1016/j.indcrop.2019.05.009
Rognli O (2013) Breeding for improved winter survival in forage grasses. In: Imai R, Yoshida M, Matsumoto N (eds) Plant and microbe adaptations to cold in a changing world. Springer, New York, pp 197–208. https://doi.org/10.1007/978-1-4614-8253-6_17
Schegoscheski Gerhardt IF, Teixeira do Amaral A Junior, Ferreira Pena G, Moreira Guimarães LJ, de Lima VJ, Vivas M, Araújo Diniz Santos PH, Alves Ferreira FR, Mendonça Freitas MS, Kamphorst SH (2019) Genetic effects on the efficiency and responsiveness to phosphorus use in popcorn as estimated by diallel analysis. PLoS ONE 14(5):e0216980. https://doi.org/10.1371/journal.pone.0216980
Shahadati-Moghaddam Z, Hosseini A, Soorni J, Trojak-Goluch A (2016) Development of tobacco (Nicotiana tabacum L.) doubled haploid lines resistant to potato virus Y0. Indian J Genet 76(3):333–340. https://doi.org/10.5958/0975-6906.2016.00050.X
Sharma JR (2006) Statistical and biometrical techniques in plant breeding. New Age International, Delhi
Skinner DZ (2012) Genetics of winter wheat response to two freezing treatments. Plant Breed 131:380–384. https://doi.org/10.1111/j.1439-0523.2012.01954.x
Skinner DZ, Garland-Campbell KA (2008) Evidence of a major genetic factor conditioning freezing sensitivity in winter wheat. Plant Breed 127:228–234. https://doi.org/10.1111/j.1439-0523.2007.01464.x
Soloklui AAG, Gharaghani A, Oraguzie N, Saed-Moucheshi A (2018) Heritability and combining ability for cold hardiness from partial dialleles in Iranian pomegranate cultivars. HortScience 53:427–431. https://doi.org/10.21273/hortsci12763-17
Soorni J, Kazemitabar SK, Kahrizi D, Dehestani A, Bagheri N (2017) Screening of camelina (Camelina sativa L.) doubled haploid lines for freezing tolerance in the seedling stage. Genetika 49(1):173–181. https://doi.org/10.2298/gensr1701173s
Sutka J (2001) Genes for frost resistance in wheat. Euphytica 119:169–177. https://doi.org/10.1023/a:1017520720183
Wittenberg A, Anderson JV, Berti MT (2019) Winter and summer annual biotypes of camelina have different morphology and seed characteristics. Ind Crops Prod 135:230–237. https://doi.org/10.1016/j.indcrop.2019.04.036
Wiwart M, Kurasiak-Popowska D, Suchowilska E, Wachowska U, Stuper-Szablewska K (2019) Variation in the morphometric parameters of seeds of spring and winter genotypes of Camelina sativa (L.) Crantz. Ind Crops Prod 139:111571. https://doi.org/10.1016/j.indcrop.2019.111571
Wrucke DF, Talukder ZI, Rahman M (2020) Genome-wide association study for frost tolerance in rapeseed/canola (Brassica napus) under simulating freezing conditions. Plant Breed 139(2):356–367. https://doi.org/10.1111/pbr.12771
Xing N, Fan C, Zhou Y (2014) Parental selection of hybrid breeding based on maternal and paternal inheritance of traits in rapeseed (Brassica napus L.). PLoS ONE 9(7):e103165. https://doi.org/10.1371/journal.pone.0103165
Zelt NH, Schoen DJ (2016) Testing for heterosis in traits associated with seed yield in Camelina sativa. Can J Plant Sci 96:525–529. https://doi.org/10.1139/cjps-2015-0254
Acknowledgements
Special thanks to Dr. David Horvath from USDA-ARS for the valuable editing of the manuscript. Also, thanks to Plant Gene Resources of Canada, Science and Technology Branch Agriculture and Agri-Food Canada/Government of Canada for the donation of some parents of the camelina DH lines. The authors also wish to thank the laboratory staff of Genetics and Agricultural Biotechnology Institute of Tabarestan (GABIT), Sari Agricultural Sciences and Natural Resources University (SANRU), for their support and technical assistance.
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Soorni, J., Kazemitabar, S.K., Kahrizi, D. et al. Genetic analysis of freezing tolerance in camelina [Camelina sativa (L.) Crantz] by diallel cross of winter and spring biotypes. Planta 253, 9 (2021). https://doi.org/10.1007/s00425-020-03521-z
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DOI: https://doi.org/10.1007/s00425-020-03521-z